Nicotinamide‐N‐methyltransferase is a promising metabolic drug target for primary and metastatic clear cell renal cell carcinoma

Background The metabolic enzyme nicotinamide‐N‐methyltransferase (NNMT) is highly expressed in various cancer entities, suggesting tumour‐promoting functions. We systematically investigated NNMT expression and its metabolic interactions in clear cell renal cell carcinoma (ccRCC), a prominent RCC sub...

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Published inClinical and translational medicine Vol. 12; no. 6; pp. e883 - n/a
Main Authors Reustle, Anna, Menig, Lena‐Sophie, Leuthold, Patrick, Hofmann, Ute, Stühler, Viktoria, Schmees, Christian, Becker, Michael, Haag, Mathias, Klumpp, Verena, Winter, Stefan, Büttner, Florian A., Rausch, Steffen, Hennenlotter, Jörg, Fend, Falko, Scharpf, Marcus, Stenzl, Arnulf, Bedke, Jens, Schwab, Matthias, Schaeffeler, Elke
Format Journal Article
LanguageEnglish
Published United States John Wiley & Sons, Inc 01.06.2022
John Wiley and Sons Inc
Wiley
Subjects
Antibodies
Carcinoma, Renal Cell - drug therapy
Carcinoma, Renal Cell - genetics
Carcinoma, Renal Cell - metabolism
Clinical medicine
Deoxyglucose
DNA methylation
Enzymes
Fatty acids
Gene expression
Genomes
Glucose
Glutamine
Humans
Kidney cancer
Kidney Neoplasms - drug therapy
Kidney Neoplasms - genetics
Kidney Neoplasms - metabolism
Lymphatic system
Metabolism
Metastasis
Niacinamide - pharmacology
NNMT
NNMTi
oxphos
Patients
renal cell carcinoma
Response rates
Tumor Microenvironment
Urology
Germany
renal cell carcinoma
NNMT
metastasis
metabolism
glutamine
oxphos
NNMTi
Online AccessGet full text
ISSN2001-1326
2001-1326
DOI10.1002/ctm2.883

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Abstract Background The metabolic enzyme nicotinamide‐N‐methyltransferase (NNMT) is highly expressed in various cancer entities, suggesting tumour‐promoting functions. We systematically investigated NNMT expression and its metabolic interactions in clear cell renal cell carcinoma (ccRCC), a prominent RCC subtype with metabolic alterations, to elucidate its role as a drug target. Methods NNMT expression was assessed in primary ccRCC (n = 134), non‐tumour tissue and ccRCC‐derived metastases (n = 145) by microarray analysis and/or immunohistochemistry. Findings were validated in The Cancer Genome Atlas (kidney renal clear cell carcinoma [KIRC], n = 452) and by single‐cell analysis. Expression was correlated with clinicopathological data and survival. Metabolic alterations in NNMT‐depleted cells were assessed by nontargeted/targeted metabolomics and extracellular flux analysis. The NNMT inhibitor (NNMTi) alone and in combination with the inhibitor 2‐deoxy‐D‐glucose for glycolysis and BPTES (bis‐2‐(5‐phenylacetamido‐1,3,4‐thiadiazol‐2‐yl)ethyl‐sulfide) for glutamine metabolism was investigated in RCC cell lines (786‐O, A498) and in two 2D ccRCC‐derived primary cultures and three 3D ccRCC air–liquid interface models. Results NNMT protein was overexpressed in primary ccRCC (p = 1.32 × 10–16) and ccRCC‐derived metastases (p = 3.92 × 10–20), irrespective of metastatic location, versus non‐tumour tissue. Single‐cell data showed predominant NNMT expression in ccRCC and not in the tumour microenvironment. High NNMT expression in primary ccRCC correlated with worse survival in independent cohorts (primary RCC—hazard ratio [HR] = 4.3, 95% confidence interval [CI]: 1.5–12.4; KIRC—HR = 3.3, 95% CI: 2.0–5.4). NNMT depletion leads to intracellular glutamine accumulation, with negative effects on mitochondrial function and cell survival, while not affecting glycolysis or glutathione metabolism. At the gene level, NNMT‐depleted cells upregulate glycolysis, oxidative phosphorylation and apoptosis pathways. NNMTi alone or in combination with 2‐deoxy‐D‐glucose and BPTES resulted in inhibition of cell viability in ccRCC cell lines and primary tumour and metastasis‐derived models. In two out of three patient‐derived ccRCC air–liquid interface models, NNMTi treatment induced cytotoxicity. Conclusions Since efficient glutamine utilisation, which is essential for ccRCC tumours, depends on NNMT, small‐molecule NNMT inhibitors provide a novel therapeutic strategy for ccRCC and act as sensitizers for combination therapies. NNMT is highly expressed in ccRCC primary tumours and metastases, correlating with worse patient survival. Glutamine metabolism is impaired in NNMT‐depleted cells, with negative consequences for cellular fitness. NNMT inhibition reduces cell viability and induces cytotoxicity in 2D/3D ccRCC‐derived tumour models. Beyond NNMT inhibition for the treatment of metabolic diseases, its application for anticancer therapy appears promising.
AbstractList Abstract Background The metabolic enzyme nicotinamide‐N‐methyltransferase (NNMT) is highly expressed in various cancer entities, suggesting tumour‐promoting functions. We systematically investigated NNMT expression and its metabolic interactions in clear cell renal cell carcinoma (ccRCC), a prominent RCC subtype with metabolic alterations, to elucidate its role as a drug target. Methods NNMT expression was assessed in primary ccRCC (n = 134), non‐tumour tissue and ccRCC‐derived metastases (n = 145) by microarray analysis and/or immunohistochemistry. Findings were validated in The Cancer Genome Atlas (kidney renal clear cell carcinoma [KIRC], n = 452) and by single‐cell analysis. Expression was correlated with clinicopathological data and survival. Metabolic alterations in NNMT‐depleted cells were assessed by nontargeted/targeted metabolomics and extracellular flux analysis. The NNMT inhibitor (NNMTi) alone and in combination with the inhibitor 2‐deoxy‐D‐glucose for glycolysis and BPTES (bis‐2‐(5‐phenylacetamido‐1,3,4‐thiadiazol‐2‐yl)ethyl‐sulfide) for glutamine metabolism was investigated in RCC cell lines (786‐O, A498) and in two 2D ccRCC‐derived primary cultures and three 3D ccRCC air–liquid interface models. Results NNMT protein was overexpressed in primary ccRCC (p = 1.32 × 10–16) and ccRCC‐derived metastases (p = 3.92 × 10–20), irrespective of metastatic location, versus non‐tumour tissue. Single‐cell data showed predominant NNMT expression in ccRCC and not in the tumour microenvironment. High NNMT expression in primary ccRCC correlated with worse survival in independent cohorts (primary RCC—hazard ratio [HR] = 4.3, 95% confidence interval [CI]: 1.5–12.4; KIRC—HR = 3.3, 95% CI: 2.0–5.4). NNMT depletion leads to intracellular glutamine accumulation, with negative effects on mitochondrial function and cell survival, while not affecting glycolysis or glutathione metabolism. At the gene level, NNMT‐depleted cells upregulate glycolysis, oxidative phosphorylation and apoptosis pathways. NNMTi alone or in combination with 2‐deoxy‐D‐glucose and BPTES resulted in inhibition of cell viability in ccRCC cell lines and primary tumour and metastasis‐derived models. In two out of three patient‐derived ccRCC air–liquid interface models, NNMTi treatment induced cytotoxicity. Conclusions Since efficient glutamine utilisation, which is essential for ccRCC tumours, depends on NNMT, small‐molecule NNMT inhibitors provide a novel therapeutic strategy for ccRCC and act as sensitizers for combination therapies.
The metabolic enzyme nicotinamide-N-methyltransferase (NNMT) is highly expressed in various cancer entities, suggesting tumour-promoting functions. We systematically investigated NNMT expression and its metabolic interactions in clear cell renal cell carcinoma (ccRCC), a prominent RCC subtype with metabolic alterations, to elucidate its role as a drug target. NNMT expression was assessed in primary ccRCC (n = 134), non-tumour tissue and ccRCC-derived metastases (n = 145) by microarray analysis and/or immunohistochemistry. Findings were validated in The Cancer Genome Atlas (kidney renal clear cell carcinoma [KIRC], n = 452) and by single-cell analysis. Expression was correlated with clinicopathological data and survival. Metabolic alterations in NNMT-depleted cells were assessed by nontargeted/targeted metabolomics and extracellular flux analysis. The NNMT inhibitor (NNMTi) alone and in combination with the inhibitor 2-deoxy-D-glucose for glycolysis and BPTES (bis-2-(5-phenylacetamido-1,3,4-thiadiazol-2-yl)ethyl-sulfide) for glutamine metabolism was investigated in RCC cell lines (786-O, A498) and in two 2D ccRCC-derived primary cultures and three 3D ccRCC air-liquid interface models. NNMT protein was overexpressed in primary ccRCC (p = 1.32 × 10 ) and ccRCC-derived metastases (p = 3.92 × 10 ), irrespective of metastatic location, versus non-tumour tissue. Single-cell data showed predominant NNMT expression in ccRCC and not in the tumour microenvironment. High NNMT expression in primary ccRCC correlated with worse survival in independent cohorts (primary RCC-hazard ratio [HR] = 4.3, 95% confidence interval [CI]: 1.5-12.4; KIRC-HR = 3.3, 95% CI: 2.0-5.4). NNMT depletion leads to intracellular glutamine accumulation, with negative effects on mitochondrial function and cell survival, while not affecting glycolysis or glutathione metabolism. At the gene level, NNMT-depleted cells upregulate glycolysis, oxidative phosphorylation and apoptosis pathways. NNMTi alone or in combination with 2-deoxy-D-glucose and BPTES resulted in inhibition of cell viability in ccRCC cell lines and primary tumour and metastasis-derived models. In two out of three patient-derived ccRCC air-liquid interface models, NNMTi treatment induced cytotoxicity. Since efficient glutamine utilisation, which is essential for ccRCC tumours, depends on NNMT, small-molecule NNMT inhibitors provide a novel therapeutic strategy for ccRCC and act as sensitizers for combination therapies.
BackgroundThe metabolic enzyme nicotinamide-N-methyltransferase (NNMT) is highly expressed in various cancer entities, suggesting tumour-promoting functions. We systematically investigated NNMT expression and its metabolic interactions in clear cell renal cell carcinoma (ccRCC), a prominent RCC subtype with metabolic alterations, to elucidate its role as a drug target.MethodsNNMT expression was assessed in primary ccRCC (n = 134), non-tumour tissue and ccRCC-derived metastases (n = 145) by microarray analysis and/or immunohistochemistry. Findings were validated in The Cancer Genome Atlas (kidney renal clear cell carcinoma [KIRC], n = 452) and by single-cell analysis. Expression was correlated with clinicopathological data and survival. Metabolic alterations in NNMT-depleted cells were assessed by nontargeted/targeted metabolomics and extracellular flux analysis. The NNMT inhibitor (NNMTi) alone and in combination with the inhibitor 2-deoxy-D-glucose for glycolysis and BPTES (bis-2-(5-phenylacetamido-1,3,4-thiadiazol-2-yl)ethyl-sulfide) for glutamine metabolism was investigated in RCC cell lines (786-O, A498) and in two 2D ccRCC-derived primary cultures and three 3D ccRCC air–liquid interface models.ResultsNNMT protein was overexpressed in primary ccRCC (p = 1.32 × 10–16) and ccRCC-derived metastases (p = 3.92 × 10–20), irrespective of metastatic location, versus non-tumour tissue. Single-cell data showed predominant NNMT expression in ccRCC and not in the tumour microenvironment. High NNMT expression in primary ccRCC correlated with worse survival in independent cohorts (primary RCC—hazard ratio [HR] = 4.3, 95% confidence interval [CI]: 1.5–12.4; KIRC—HR = 3.3, 95% CI: 2.0–5.4). NNMT depletion leads to intracellular glutamine accumulation, with negative effects on mitochondrial function and cell survival, while not affecting glycolysis or glutathione metabolism. At the gene level, NNMT-depleted cells upregulate glycolysis, oxidative phosphorylation and apoptosis pathways. NNMTi alone or in combination with 2-deoxy-D-glucose and BPTES resulted in inhibition of cell viability in ccRCC cell lines and primary tumour and metastasis-derived models. In two out of three patient-derived ccRCC air–liquid interface models, NNMTi treatment induced cytotoxicity.ConclusionsSince efficient glutamine utilisation, which is essential for ccRCC tumours, depends on NNMT, small-molecule NNMT inhibitors provide a novel therapeutic strategy for ccRCC and act as sensitizers for combination therapies.
Background The metabolic enzyme nicotinamide‐N‐methyltransferase (NNMT) is highly expressed in various cancer entities, suggesting tumour‐promoting functions. We systematically investigated NNMT expression and its metabolic interactions in clear cell renal cell carcinoma (ccRCC), a prominent RCC subtype with metabolic alterations, to elucidate its role as a drug target. Methods NNMT expression was assessed in primary ccRCC (n = 134), non‐tumour tissue and ccRCC‐derived metastases (n = 145) by microarray analysis and/or immunohistochemistry. Findings were validated in The Cancer Genome Atlas (kidney renal clear cell carcinoma [KIRC], n = 452) and by single‐cell analysis. Expression was correlated with clinicopathological data and survival. Metabolic alterations in NNMT‐depleted cells were assessed by nontargeted/targeted metabolomics and extracellular flux analysis. The NNMT inhibitor (NNMTi) alone and in combination with the inhibitor 2‐deoxy‐D‐glucose for glycolysis and BPTES (bis‐2‐(5‐phenylacetamido‐1,3,4‐thiadiazol‐2‐yl)ethyl‐sulfide) for glutamine metabolism was investigated in RCC cell lines (786‐O, A498) and in two 2D ccRCC‐derived primary cultures and three 3D ccRCC air–liquid interface models. Results NNMT protein was overexpressed in primary ccRCC (p = 1.32 × 10–16) and ccRCC‐derived metastases (p = 3.92 × 10–20), irrespective of metastatic location, versus non‐tumour tissue. Single‐cell data showed predominant NNMT expression in ccRCC and not in the tumour microenvironment. High NNMT expression in primary ccRCC correlated with worse survival in independent cohorts (primary RCC—hazard ratio [HR] = 4.3, 95% confidence interval [CI]: 1.5–12.4; KIRC—HR = 3.3, 95% CI: 2.0–5.4). NNMT depletion leads to intracellular glutamine accumulation, with negative effects on mitochondrial function and cell survival, while not affecting glycolysis or glutathione metabolism. At the gene level, NNMT‐depleted cells upregulate glycolysis, oxidative phosphorylation and apoptosis pathways. NNMTi alone or in combination with 2‐deoxy‐D‐glucose and BPTES resulted in inhibition of cell viability in ccRCC cell lines and primary tumour and metastasis‐derived models. In two out of three patient‐derived ccRCC air–liquid interface models, NNMTi treatment induced cytotoxicity. Conclusions Since efficient glutamine utilisation, which is essential for ccRCC tumours, depends on NNMT, small‐molecule NNMT inhibitors provide a novel therapeutic strategy for ccRCC and act as sensitizers for combination therapies. NNMT is highly expressed in ccRCC primary tumours and metastases, correlating with worse patient survival. Glutamine metabolism is impaired in NNMT‐depleted cells, with negative consequences for cellular fitness. NNMT inhibition reduces cell viability and induces cytotoxicity in 2D/3D ccRCC‐derived tumour models. Beyond NNMT inhibition for the treatment of metabolic diseases, its application for anticancer therapy appears promising.
NNMT is highly expressed in ccRCC primary tumours and metastases, correlating with worse patient survival. Glutamine metabolism is impaired in NNMT‐depleted cells, with negative consequences for cellular fitness. NNMT inhibition reduces cell viability and induces cytotoxicity in 2D/3D ccRCC‐derived tumour models. Beyond NNMT inhibition for the treatment of metabolic diseases, its application for anticancer therapy appears promising.
The metabolic enzyme nicotinamide-N-methyltransferase (NNMT) is highly expressed in various cancer entities, suggesting tumour-promoting functions. We systematically investigated NNMT expression and its metabolic interactions in clear cell renal cell carcinoma (ccRCC), a prominent RCC subtype with metabolic alterations, to elucidate its role as a drug target.BACKGROUNDThe metabolic enzyme nicotinamide-N-methyltransferase (NNMT) is highly expressed in various cancer entities, suggesting tumour-promoting functions. We systematically investigated NNMT expression and its metabolic interactions in clear cell renal cell carcinoma (ccRCC), a prominent RCC subtype with metabolic alterations, to elucidate its role as a drug target.NNMT expression was assessed in primary ccRCC (n = 134), non-tumour tissue and ccRCC-derived metastases (n = 145) by microarray analysis and/or immunohistochemistry. Findings were validated in The Cancer Genome Atlas (kidney renal clear cell carcinoma [KIRC], n = 452) and by single-cell analysis. Expression was correlated with clinicopathological data and survival. Metabolic alterations in NNMT-depleted cells were assessed by nontargeted/targeted metabolomics and extracellular flux analysis. The NNMT inhibitor (NNMTi) alone and in combination with the inhibitor 2-deoxy-D-glucose for glycolysis and BPTES (bis-2-(5-phenylacetamido-1,3,4-thiadiazol-2-yl)ethyl-sulfide) for glutamine metabolism was investigated in RCC cell lines (786-O, A498) and in two 2D ccRCC-derived primary cultures and three 3D ccRCC air-liquid interface models.METHODSNNMT expression was assessed in primary ccRCC (n = 134), non-tumour tissue and ccRCC-derived metastases (n = 145) by microarray analysis and/or immunohistochemistry. Findings were validated in The Cancer Genome Atlas (kidney renal clear cell carcinoma [KIRC], n = 452) and by single-cell analysis. Expression was correlated with clinicopathological data and survival. Metabolic alterations in NNMT-depleted cells were assessed by nontargeted/targeted metabolomics and extracellular flux analysis. The NNMT inhibitor (NNMTi) alone and in combination with the inhibitor 2-deoxy-D-glucose for glycolysis and BPTES (bis-2-(5-phenylacetamido-1,3,4-thiadiazol-2-yl)ethyl-sulfide) for glutamine metabolism was investigated in RCC cell lines (786-O, A498) and in two 2D ccRCC-derived primary cultures and three 3D ccRCC air-liquid interface models.NNMT protein was overexpressed in primary ccRCC (p = 1.32 × 10-16 ) and ccRCC-derived metastases (p = 3.92 × 10-20 ), irrespective of metastatic location, versus non-tumour tissue. Single-cell data showed predominant NNMT expression in ccRCC and not in the tumour microenvironment. High NNMT expression in primary ccRCC correlated with worse survival in independent cohorts (primary RCC-hazard ratio [HR] = 4.3, 95% confidence interval [CI]: 1.5-12.4; KIRC-HR = 3.3, 95% CI: 2.0-5.4). NNMT depletion leads to intracellular glutamine accumulation, with negative effects on mitochondrial function and cell survival, while not affecting glycolysis or glutathione metabolism. At the gene level, NNMT-depleted cells upregulate glycolysis, oxidative phosphorylation and apoptosis pathways. NNMTi alone or in combination with 2-deoxy-D-glucose and BPTES resulted in inhibition of cell viability in ccRCC cell lines and primary tumour and metastasis-derived models. In two out of three patient-derived ccRCC air-liquid interface models, NNMTi treatment induced cytotoxicity.RESULTSNNMT protein was overexpressed in primary ccRCC (p = 1.32 × 10-16 ) and ccRCC-derived metastases (p = 3.92 × 10-20 ), irrespective of metastatic location, versus non-tumour tissue. Single-cell data showed predominant NNMT expression in ccRCC and not in the tumour microenvironment. High NNMT expression in primary ccRCC correlated with worse survival in independent cohorts (primary RCC-hazard ratio [HR] = 4.3, 95% confidence interval [CI]: 1.5-12.4; KIRC-HR = 3.3, 95% CI: 2.0-5.4). NNMT depletion leads to intracellular glutamine accumulation, with negative effects on mitochondrial function and cell survival, while not affecting glycolysis or glutathione metabolism. At the gene level, NNMT-depleted cells upregulate glycolysis, oxidative phosphorylation and apoptosis pathways. NNMTi alone or in combination with 2-deoxy-D-glucose and BPTES resulted in inhibition of cell viability in ccRCC cell lines and primary tumour and metastasis-derived models. In two out of three patient-derived ccRCC air-liquid interface models, NNMTi treatment induced cytotoxicity.Since efficient glutamine utilisation, which is essential for ccRCC tumours, depends on NNMT, small-molecule NNMT inhibitors provide a novel therapeutic strategy for ccRCC and act as sensitizers for combination therapies.CONCLUSIONSSince efficient glutamine utilisation, which is essential for ccRCC tumours, depends on NNMT, small-molecule NNMT inhibitors provide a novel therapeutic strategy for ccRCC and act as sensitizers for combination therapies.
Author Rausch, Steffen
Stenzl, Arnulf
Klumpp, Verena
Hennenlotter, Jörg
Hofmann, Ute
Scharpf, Marcus
Schaeffeler, Elke
Schmees, Christian
Reustle, Anna
Leuthold, Patrick
Menig, Lena‐Sophie
Stühler, Viktoria
Bedke, Jens
Schwab, Matthias
Fend, Falko
Winter, Stefan
Becker, Michael
Büttner, Florian A.
Haag, Mathias
AuthorAffiliation 5 Experimental Pharmacology and Oncology GmbH Berlin‐Buch Germany
3 Department of Urology University Hospital Tuebingen Tuebingen Germany
7 German Cancer Consortium (DKTK), Partner Site Tübingen German Cancer Research Center (DKFZ) Heidelberg Germany
4 NMI Natural and Medical Sciences Institute at the University of Tuebingen Reutlingen Germany
6 Institute of Pathology and Neuropathology University Hospital Tuebingen Tuebingen Germany
2 University of Tuebingen Tuebingen Germany
1 Dr. Margarete Fischer‐Bosch Institute of Clinical Pharmacology Stuttgart Germany
8 Departments of Clinical Pharmacology, Pharmacy and Biochemistry University of Tuebingen Tuebingen Germany
9 Cluster of Excellence iFIT (EXC2180) ‘Image‐Guided and Functionally Instructed Tumor Therapies’ University of Tuebingen Tuebingen Germany
AuthorAffiliation_xml – name: 6 Institute of Pathology and Neuropathology University Hospital Tuebingen Tuebingen Germany
– name: 1 Dr. Margarete Fischer‐Bosch Institute of Clinical Pharmacology Stuttgart Germany
– name: 7 German Cancer Consortium (DKTK), Partner Site Tübingen German Cancer Research Center (DKFZ) Heidelberg Germany
– name: 9 Cluster of Excellence iFIT (EXC2180) ‘Image‐Guided and Functionally Instructed Tumor Therapies’ University of Tuebingen Tuebingen Germany
– name: 5 Experimental Pharmacology and Oncology GmbH Berlin‐Buch Germany
– name: 4 NMI Natural and Medical Sciences Institute at the University of Tuebingen Reutlingen Germany
– name: 2 University of Tuebingen Tuebingen Germany
– name: 3 Department of Urology University Hospital Tuebingen Tuebingen Germany
– name: 8 Departments of Clinical Pharmacology, Pharmacy and Biochemistry University of Tuebingen Tuebingen Germany
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  surname: Reustle
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  organization: University of Tuebingen
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  organization: University of Tuebingen
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  organization: University of Tuebingen
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  surname: Hofmann
  fullname: Hofmann, Ute
  organization: University of Tuebingen
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  givenname: Viktoria
  surname: Stühler
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  organization: University Hospital Tuebingen
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  surname: Schmees
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  organization: NMI Natural and Medical Sciences Institute at the University of Tuebingen
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  surname: Haag
  fullname: Haag, Mathias
  organization: University of Tuebingen
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  surname: Klumpp
  fullname: Klumpp, Verena
  organization: University of Tuebingen
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  fullname: Winter, Stefan
  organization: University of Tuebingen
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  givenname: Florian A.
  surname: Büttner
  fullname: Büttner, Florian A.
  organization: University of Tuebingen
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  givenname: Steffen
  surname: Rausch
  fullname: Rausch, Steffen
  organization: University Hospital Tuebingen
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  organization: University Hospital Tuebingen
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  organization: University Hospital Tuebingen
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  fullname: Scharpf, Marcus
  organization: University Hospital Tuebingen
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  givenname: Arnulf
  surname: Stenzl
  fullname: Stenzl, Arnulf
  organization: University Hospital Tuebingen
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  givenname: Jens
  surname: Bedke
  fullname: Bedke, Jens
  organization: German Cancer Research Center (DKFZ)
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  givenname: Matthias
  orcidid: 0000-0002-9984-075X
  surname: Schwab
  fullname: Schwab, Matthias
  email: matthias.schwab@ikp-stuttgart.de
  organization: University of Tuebingen
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  surname: Schaeffeler
  fullname: Schaeffeler, Elke
  organization: University of Tuebingen
BackLink https://www.ncbi.nlm.nih.gov/pubmed/35678045$$D View this record in MEDLINE/PubMed
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Copyright 2022 The Authors. published by John Wiley & Sons Australia, Ltd on behalf of Shanghai Institute of Clinical Bioinformatics.
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Issue 6
Keywords renal cell carcinoma
NNMT
metastasis
metabolism
glutamine
oxphos
NNMTi
Language English
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2022 The Authors. Clinical and Translational Medicine published by John Wiley & Sons Australia, Ltd on behalf of Shanghai Institute of Clinical Bioinformatics.
This is an open access article under the terms of the http://creativecommons.org/licenses/by/4.0/ License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.
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Notes Funding information
Matthias Schwab and Elke Schaeffeler contributed equally.
Robert Bosch Stiftung (Stuttgart, Germany); Deutsche Forschungsgemeinschaft (DFG, German Research Foundation) under Germany's Excellence Strategy (EXC 2180—390900677); ICEPHA Graduate School Tuebingen‐Stuttgart.
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Snippet Background The metabolic enzyme nicotinamide‐N‐methyltransferase (NNMT) is highly expressed in various cancer entities, suggesting tumour‐promoting functions....
The metabolic enzyme nicotinamide-N-methyltransferase (NNMT) is highly expressed in various cancer entities, suggesting tumour-promoting functions. We...
BackgroundThe metabolic enzyme nicotinamide-N-methyltransferase (NNMT) is highly expressed in various cancer entities, suggesting tumour-promoting functions....
NNMT is highly expressed in ccRCC primary tumours and metastases, correlating with worse patient survival. Glutamine metabolism is impaired in NNMT‐depleted...
Abstract Background The metabolic enzyme nicotinamide‐N‐methyltransferase (NNMT) is highly expressed in various cancer entities, suggesting tumour‐promoting...
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StartPage e883
SubjectTerms Antibodies
Carcinoma, Renal Cell - drug therapy
Carcinoma, Renal Cell - genetics
Carcinoma, Renal Cell - metabolism
Clinical medicine
Deoxyglucose
DNA methylation
Enzymes
Fatty acids
Gene expression
Genomes
Glucose
Glutamine
Humans
Kidney cancer
Kidney Neoplasms - drug therapy
Kidney Neoplasms - genetics
Kidney Neoplasms - metabolism
Lymphatic system
Metabolism
Metastasis
Niacinamide - pharmacology
NNMT
NNMTi
oxphos
Patients
renal cell carcinoma
Response rates
Tumor Microenvironment
Urology
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Title Nicotinamide‐N‐methyltransferase is a promising metabolic drug target for primary and metastatic clear cell renal cell carcinoma
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